Converging Light, Energy and Hormonal Signaling Control Meristem Activity, Leaf Initiation, and Growth

Abstract

The development of leaf primordia is subject to light control of meristematic activity. Light regulates the expression of thousands of genes with roles in cell proliferation, organ development, and differentiation of photosynthetic cells. Previous work has highlighted roles for hormone homeostasis and the energy-dependent Target of Rapamycin (TOR) kinase in meristematic activity, yet a picture of how these two regulatory mechanisms depend on light perception and interact with each other has yet to emerge. Their relevance beyond leaf initiation also is unclear. Here, we report the discovery that the dark-arrested meristematic region of Arabidopsis () experiences a local energy deprivation state and confirm previous findings that the PIN1 auxin transporter is diffusely localized in the dark. Light triggers a rapid removal of the starvation state and the establishment of PIN1 polar membrane localization consistent with auxin export, both preceding the induction of cell cycle- and cytoplasmic growth-associated genes. We demonstrate that shoot meristematic activity can occur in the dark through the manipulation of auxin and cytokinin activity as well as through the activation of energy signaling, both targets of photomorphogenesis action, but the organ developmental outcomes differ: while TOR-dependent energy signals alone stimulate cell proliferation, the development of a normal leaf lamina requires photomorphogenesis-like hormonal responses. We further show that energy signaling adjusts the extent of cell cycle activity and growth of young leaves non-cellautonomously to available photosynthates and leads to organs constituted of a greater number of cells developing under higher irradiance. This makes energy signaling perhaps the most important biomass growth determinant under natural, unstressed conditions.

Multiple steps of leaf thickening during sun‐leaf formation in Arabidopsis

“…Sucrose stimulates the cell cycle via Dtype cyclins and target of rapamycin1 (TOR1) kinase, which are activated in both the mitotic cycle and the endocycle (Khamlichi et al, 2000;Menges et al, 2006;Dewitte et al, 2007;Velappan et al, 2017). Additionally, sucrose is highly synthesized in mature leaves under HL conditions in Arabidopsis and has been proposed as a candidate systemic signal for sun-leaf induction (Terashima et al, 2005;J€ ank€ anp€ a€ a et al, 2012;Mohammed et al, 2018).…”

“…In sun leaves of Arabidopsis, cells in the palisade mesophyll are larger than those in shade leaves through anisotropic elongation in the dorsoventral direction under HL conditions (Wuyts et al, 2012). Also, HL irradiation of LLgrown seedlings promotes the endocycle (Mohammed et al, 2018), but whether endocycle progression is responsible for anisotropic cell elongation in sun leaves is unknown. This is because of the scarcity of basic information on leafthickness growth, in contrast to that gleaned from extensive studies on paradermal growth in leaves (Tsuge et al, 1996;Donnelly et al, 1999;Yano and Terashima, 2004;Tsukaya, 2013;Kalve et al, 2014;Chitwood et al, 2015).…”

Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

“…Recent reports involving TOR inhibitor treatment have indicated that these effects could be due to transcriptional downregulation of genes encoding plastidic ribosomal proteins and photosynthetic proteins as well as those of the tetrapyrrole biosynthesis pathway in Arabidopsis (Dobrenel, Mancera‐Martínez, et al, ; Dong et al, ). Thus, the TORC1 complex has been shown to play a crucial role in biogenesis and maturation of chloroplast to promote leaf and cotyledon greening (Li, Gao, Xue, Wang, & Zhao, ; Li, Song, et al, ; Mohammed et al, ; Sun et al, ; Zhang et al, ). Moreover, reports have also indicated that TOR kinase plays an important role in phytohormone signaling including that of auxin, gibberellic acid, brassinosteroids, and cytokinins etc (Li & Sheen, ; Quilichini et al, ; Wang et al, ; Wu et al, ; Xiong et al, ; Zhang et al, ).…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…Whereas TOR can integrate sugar and auxin signals (Schepetilnikov and Ryabova, 2018) to stimulate cell proliferation, photomorphogenesis is required for formation of the leaf lamina (Mohammed et al, 2018). Shoot branching is another developmental process that relies on energy supply in the form of sugars.…”

“…How energy signaling controls leaf initiation and expansion is explored by Mohammed et al (2018), who demonstrate the importance of integration of multiple energy signals, including light, Suc, and hormones. Whereas TOR can integrate sugar and auxin signals (Schepetilnikov and Ryabova, 2018) to stimulate cell proliferation, photomorphogenesis is required for formation of the leaf lamina (Mohammed et al, 2018).…”